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1.15Citrus peelminer [Lepidoptera: Gracillariidae]

Marmara gulosa

Marmara gulosa is not recorded from Western Australia and so is a pest of quarantine concern for that state.

Marmara gulosa is a moth native to the southwestern USA and has become an economic pest in California, Arizona, Cuba and Mexico (Guillén et al. 2001; Jones 2001). It was first misidentified as M. salictella on the young twigs of willow in the Atlantic states but was subsequently described as M. gulosa (Guillén et al. 2001). It probably initially attacked willow, but has undergone a host shift to various plants not native to the USA including citrus and oleander (Jones 2001).

In California, M. gulosa was first reported on citrus in 1917 and as a sporadic pest up until the 1970s (Kirkland 2009). High populations were recorded from the Coachella Valley in the mid 1980s and mid 1990s, and in 1999 M. gulosa was reported from the southern San Joaquin Valley with high infestations apparent by 2000 (Kirkland 2009). It is recorded throughout southern and central California, including desert areas (Jones 2001; Grafton-Cardwell et al. 2008).

Marmara gulosa is a highly polyphagous pest which is reported to feed on hosts from up to 31 plant families including fruit and vegetable crops; ornamentals; and weeds (Grafton-Cardwell 2002; Kirkland 2009). In commercial production, it is primarily a pest of citrus, especially grapefruit and navel oranges; however, infestations have been observed on cotton, cowpeas, eggplant, grape, capsicum, plum, pumpkin and zucchini (Stelinski 2007).

In the San Joaquin Valley citrus, table grapes and nursery stock have been most affected by M. gulosa (Grafton-Cardwell et al. 2003). It has been found heavily infesting table grapes, in which it attacked stems and fruit of varieties with large berries (Grafton-Cardwell et al. 2003). It has also been reported on petioles, tendrils and bunch rachises (Eichlin and Kinnee 2001).

Larvae of M. gulosa cause economic damage by feeding on the upper epidermal layers of the fruit, creating a silvery white serpentine surface mine (Kirkland 2009). Under high pest pressures, mining of leaves is observed also (Grafton-Cardwell et al. 2012). Fruit damage is considered cosmetic but the occurrence of a single mine can render the fruit unacceptable for sale (Grafton-Cardwell et al. 2012). In citrus, it can cause from 5 to 80% loss of marketable fruit in susceptible varieties (Grafton-Cardwell et al. 2012). An outbreak of M. gulosa in the Coachella Valley in 1995 caused 80-90% marketable fruit losses in some areas (Stelinski 2007).

The risk scenario of concern for M. gulosa is the presence of eggs, larvae or adults within bunches of imported table grapes.

1.15.1Probability of entry

The probability of entry is considered in two parts, the probability of importation and the probability of distribution, which consider pre-border and post-border issues, respectively.

Probability of importation

The likelihood that Marmara gulosa will arrive in Western Australia with the importation of table grapes from California is: MODERATE.

Supporting information for this assessment is provided below:

• 
  Marmara gulosa is native to the USA and has become an economically important pest in California, particularly of citrus in the Coachella and San Joaquin Valleys (Stelinski 2007; Grafton-Cardwell et al. 2012).
  
• 
  Anecdotal evidence suggest that M. gulosa has entered California from Mexico on shipments of citrus and caused outbreaks of the pest in California (Kirkland 2009). This suggests that the pest can be spread through trade of horticultural products, although this was not on table grapes
  
• 
  Often, M. gulosa populations build in grape or cotton crops and disperse into neighbouring citrus orchards when the fruit begins to senesce (Grafton-Cardwell et al. 2003).
  
• 
  On grapes, infestation has been reported on the stem, petiole, tendril, bunch rachis and berries (Eichlin and Kinnee 2001; Grafton-Cardwell et al. 2003).
  
• 
  In California, citrus, table grapes and nursery stock have been most affected by M. gulosa; and in 2001 citrus and table grape shipments from California were rejected by trading partners due to interceptions of M. gulosa (Grafton-Cardwell et al. 2003).
  
• 
  Eggs are deposited on stems and fruits and the larvae feed on the upper epidermal layers of fruit (Grafton-Cardwell et al. 2008). Eggs can be present on grape bunches and go undetected.
  
• 
  The mining caused by M. gulosa larvae blemishes the surface of fruit (Grafton-Cardwell et al. 2008). Where symptoms of infestation are obvious, these fruit would likely be culled during standard harvest and post-harvest quality assurance procedures as well as be detected during routine in-field pre-harvest surveillance programs. Where the damage is not visible from the outside of the bunch, it may go undetected.
  
• 
  Just before pupating, the larvae leave their mines and spin a cocoon on a twig, leaf, bark crevice, amongst trash on the ground or fruit where they pupate(Kerns et al. 2004; Grafton-Cardwell et al. 2008). Cocoons are decoarated with small white silk balls, which makes them conspicuous (Grafton-Cardwell et al. 2008); if present on grape bunches they are likely to be detected unless they are secreted within the bunch.
  
• 
  In the San Joaquin Valley, there may be 7 generations per year (Grafton-Cardwell et al. 2008) although up to 13 generations are also reported (Jones 2001). Development continues throughout the year and no overwintering stage is observed (Grafton-Cardwell et al. 2008). When plants such as citrus are dormant, the pest probably survives on adjacent plants in gardens, road side plantings and natural areas. Oleander, which is common in California, is an alternative host for this pest (Guillén et al. 2001) from which M. gulosa may invade orchards.
  
• 
  Under laboratory conditions, average fecundity was reported as 48.5 eggs per female with an average of 4.5 eggs laid per day (Guillén et al. 2001). But females are reported to lay between 10 and 50 eggs generally (Kerns et al. 2004). Given the potential fecundity and multiple generations, M. gulosa are likely to be present at the time of harvest in all life stages.
  
• 
  In 2001 shipments of table grapes from the San Joaquin Valley were rejected by foreign countries due to infestation with M. gulosa (Grafton-Cardwell et al. 2003).
  
• 
  The eggs are only 0.41 mm long and 0.28 mm wide (Guillén et al. 2001), and may be difficult to detect on a grape bunch.
  
• 
  Development is temperature-dependent and can range from two to four weeks (Kirkland 2009). O’Neal et al. (2011) reported that temperatures of 17^oC and 21^oC resulted in around 70% mortality, but required 27 and 49 days respectively to achieve this level of mortality. Similarly, the authors reported that at 17^oC or 33^oC, M. gulosa experienced greater than 10% mortality during the egg, first larval instar and second larval instar stages. Transport of table grapes from California to Australia is predominantly by air freight and the time taken from harvest to retail sale can be less than two weeks. Although some mortality to egg and larval stages may be experienced during cold treatment storage and transport, it is possible that viable M. gulosa eggs, larvae, pupae or adults could arrive in Western Australia if they are present on table grape bunches when packed in California. Where table grapes are shipped by sea freight, taking up to 3 weeks (or 4-5 weeks including post-harvest and on-arrival processing), the longer transit period could result in a higher mortality rate but would not likely preclude the potential import of viable M. gulosa life stages.
  

The presence of the pest in California throughout the year, its demonstrated association with table grape bunches, adult longevity and probable history of spread into California on citrus from Mexico are moderated by the conspicuous nature of the larval damage and cocoons, and lack of any official detection records during inspection of table grapes from California into eastern Australia. This supports a likelihood estimate for importation of ‘moderate’.

Probability of distribution

The likelihood that Marmara gulosa will be distributed within Western Australia in a viable state as a result of the processing, sale or disposal of table grapes from California and subsequently transfer to a susceptible part of a host is: HIGH.

Supporting information for this assessment is provided below:

• 
  Any eggs, larvae or pupae present on table grapes imported from California would be distributed with the commodity to destination points. Following pupation, adults are capable of independent flight and could potentially locate a suitable host from markets, repacking facilities, retailers, during transportation, or wherever they are taken by consumers. However, a review of the literature did not indicate what the dispersal range of adult M. gulosa moths is.
  
• 
  The entire life cycle takes around 30 days for completion (Kerns et al. 2004), although development is temperature-dependent and can range from two to four weeks (Kirkland 2009). Larvae pass through 4-5 instar stages which each require around 3 days for completion (Kerns et al. 2004). Adult females survive for an average of 10.9 days and males 9.3 days (Guillén et al. 2001). This suggests that they could be distributed alive on table grapes after introduction.
  
• 
  Marmara gulosa is highly polyphagous and feeds on a range of fruit and vegetable crops, ornamentals and weeds in up to 31 plant families (Grafton-Cardwell 2002; Kirkland 2009). Grafton-Cardwell et al. (2002) documented 67 hosts based on observations from infestations in Fresno, Tulare and Kern counties and Kirkland (2009) reported a host plant list of 69 species. The species is also considered to have shifted from willow to plants such as citrus and oleander (Jones 2001) indicating an ability to expand its host plant range in new environments.
  
• 
  As discussed in the introduction to this chapter, consumers may discard the waste from Californian table grapes onto household compost piles. Given that the adults of this pest can fly, there is some risk that adults could distribute to a suitable host via this pathway. However, the proportion of table grape bunch waste going to household compost is low. Consumers may also discard waste onto roadsides or other uncontrolled environments, where distribution to suitable hosts could occur.
  

This pest has a wide host range, the adults can fly and their life cycle can take up to around 30 days. This supports a likelihood risk estimate for distribution of ‘high’.

Overall probability of entry (importation  distribution)

The overall probability of entry is determined by combining the probabilities of importation and of distribution using the matrix of rules shown in Table 2.2.

The likelihood that Marmara gulosa will enter Western Australia as a result of trade in table grapes from the California and be distributed in a viable state to a susceptible host is: MODERATE.

1.15.2Probability of establishment

The likelihood that Marmara gulosa will establish within Western Australia, based on a comparison of factors in the source and destination areas that affect pest survival and reproduction is: HIGH.

Supporting information for this assessment is provided below:

• 
  The wide host range of M. gulosa suggests that it is likely, if the pest has been distributed to a suitable part of a host plant, that the host would be suitable for egg laying and larval development. As indicated, this species has probably shifted from native hosts such as willow to plants such as citrus and oleander (Jones 2001). It may be able to move to other hosts in new environments.
  
• 
  Marmara gulosa is native to southern USA and has been reported from California, Texas, Arizona, Florida, Northern Mexico and Cuba (Stelinski 2007). Many of the areas where M. gulosa has been reported share similar climates to parts of Western Australia. It is likely that warmer areas in Western Australia would be suitable for the establishment of this species.
  
• 
  Marmara gulosa can have up to 13 generations per year (Jones 2001). On average, females lay between 10 and 50 eggs (Kerns et al. 2004). The generation time varies from two to four weeks (Kirkland 2009), although it generally takes about 30 days (Kerns et al. 2004). Given the fecundity of females, a population could establish from a single gravid female. In addition, the rapid generation times would favour the establishment of M. gulosa in Western Australia should it be introduced.
  
• 
  There are currently only limited biological and cultural control measures available to manage M. gulosa. Chemical coverage can be incomplete due to: M. gulosa entering an orchard or vineyard in waves; fruit expanding rapidly leaving untreated surfaces for egg deposition; eggs being preferentially laid on low lying internal fruit; and the limited ability to penetrate inside the mines of larvae (Grafton-Cardwell et al. 2003; Grafton-Cardwell et al. 2012). Biological control has shown some success with the native eulophid wasp (Cirrospilus coachellae) in the Coachella Valley, but the wasp is unable to survive the colder winters in northern regions such as the San Joaquin Valley (Stelinski 2007; Grafton-Cardwell et al. 2012) and efforts to establish it there have been unsuccessful (Grafton-Cardwell et al. 2008). If M. gulosa was introduced, it is unlikely that suitable controls could be applied in urban areas. Also, existing IPM strategies applied in rural and horticultural areas are unlikely to be effective in limiting the establishment of this pest in Western Australia.
  

The wide host range, current geographic distribution, high reproductive potential, and limited effectiveness of current control methods support a likelihood estimate for establishment of ‘high’.

1.15.3Probability of spread

The likelihood that Marmara gulosa will spread within Western Australia, based on a comparison of factors in the source and destination areas that affect the expansion of the geographic distribution of the pest is: MODERATE.

Supporting information for this assessment is provided below:

• 
  The polyphagous nature of M. gulosa would enable it to locate suitable hosts in new areas and facilitate the spread of this pest should it be introduced and become established. It may also be able to spread to new hosts as probably occurred in California with the shift from willow to citrus (Jones 2001).
  
• 
  The current geographic distribution of M. gulosa includes California, Texas, Arizona, Florida, northern Mexico and Cuba (Stelinski 2007). Many of these areas share similar climates to parts of Western Australia and M. gulosa could spread through areas with a suitable climate; probably warmer regions of Western Australia.
  
• 
  The first collections of M. gulosa in the USA were made in 1915 from California according to Jones (2001) and 1917 according to Kirkland (2009). Only sporadic occurrences were reported in California up to the mid 1990s and M. gulosa was considered a minor pest of citrus in the San Joaquin Valley (Grafton-Cardwell et al. 2003; Kirkland 2009). Since that time, M. gulosa has rapidly spread throughout the San Joaquin Valley and to additional regions of California and the USA, infesting not only citrus, but a wide range of hosts that it had previously only rarely attacked (Grafton-Cardwell et al. 2003). This change coincides with shipments of citrus fruit from northern Mexico in response to shortages in fruit production in California in the late 1990s (Kirkland 2009). Although M. gulosa has managed to spread throughout California, the limited and disparate spread of M. gulosa in the USA and the Americas suggest there may be additional factors outside of pest management practices that impede the widespread dispersal of this pest, particularly across the southern states of the USA which may relate to host availability and climate.
  
• 
  Marmara gulosa adult moths are capable of independent flight and could disperse locally. Natural barriers such as deserts, mountains or large areas where hosts are not present would limit its ability to disperse between some areas. The long distances between production areas in Australia may reduce the likelihood that M. gulosa would disperse unaided from one agricultural region to another.
  
• 
  Long distance spread would probably rely on facilitated distribution with commodities or conveyances. The small size of eggs and larvae could enable the spread of M. gulosa to new areas undetected. However, where obvious symptoms of infestation are apparent, interstate control measures may restrict spread in a commercial context.
  
• 
  The potential fecundity of gravid females, many generations per year and potential persistence year round, would favour the spread of M. gulosa in Western Australia.
  

The wide host range, possible history of spread on Mexican citrus, capacity for flight, and high fecundity are moderated by the history of limited spread of outbreaks in south western parts of the USA. This supports a likelihood estimate for spread of ‘moderate’.

1.15.4Overall probability of entry, establishment and spread

The overall probability of entry, establishment and spread is determined by combining the probabilities of entry, of establishment and of spread using the matrix of ‘rules’ are shown in Table 2.2.

The likelihood that Marmara gulosa will enter Western Australia as a result of trade in table grapes from California, be distributed in a viable state to a susceptible host, establish in Western Australia and subsequently spread within Western Australia is: LOW.

1.15.5Consequences

The consequences of the establishment of Marmara gulosa in Western Australia have been estimated according to the methods described in Table 2.3.

Based on the decision rules described in Table 2.4, that is, where the consequences of a pest with respect to one or more criteria are ‘D’, the overall consequences are estimated to be LOW.

Reasoning for these ratings is provided below:

Criterion	Estimate and rationale
Direct
Plant life or health	D – Significant at the district level Marmara gulosa can cause direct damage to crops in the form of mines on the surface of fruit. Although the presence of mines causes only a cosmetic effect and does not damage the internal flesh, it can render fruit unmarketable in some crops. Mining damage can also cause secondary infections such as bunch rot in table grapes (Kirkland 2009). Whilst the damage is cosmetic and the interior fruit flesh remains unaffected, the presence of a single mine can render the fruit unmarketable in some commodities such as citrus (Grafton-Cardwell et al. 2008; Grafton-Cardwell et al. 2012). In citrus, significant economic impacts have been recorded in the USA, with up to 80-90% losses on marketable fruit reported in some varieties (Jones 2001; Stelinski 2007). Susceptible citrus varieties can experience damage in the range of 5-80% with other varieties rarely incurring losses of more than 3% (Grafton-Cardwell et al. 2012). Marmara gulosa is rarely considered an economic problem with other hosts (Grafton-Cardwell et al. 2012). In contrast to citrus, larval mining in crops such as cotton or grapes can cause little to no economic damage (Grafton-Cardwell et al. 2008). There are currently only limited biological and cultural control measures available to manage M. gulosa populations. Chemical coverage can be incomplete due to: numerous generations of M. gulosa entering an orchard or vineyard in waves; fruit expanding rapidly leaving untreated surfaces for egg deposition; eggs being preferentially laid on low lying internal fruit; and the limited ability to penetrate inside the mines and kill larvae (Grafton-Cardwell et al. 2003; Grafton-Cardwell et al. 2012). Biological control has shown some success, particularly with the native eulophid wasp (Cirrospilus coachellae) in the Coachella Valley, but it is unable to survive the colder winters in northern regions such as the San Joaquin Valley (Stelinski 2007; Grafton-Cardwell et al. 2012) and efforts to establish it there have been unsuccessful (Grafton-Cardwell et al. 2008).
Other aspects of the environment	A – Indiscernible at the district level There are no documented direct impacts of M. gulosa on any other aspect of the environment. Their introduction into a new environment may lead to competition for resources with native species, but there is no documented history of this occurring. The potential for some impact on plant health suggests that there may be impacts on amenity plants and ecological communities, but as stated, this has not been documented.
Indirect
Eradication, control etc.	D – Significant at the district level Current pest management practices and biological control activities have had only limited success in controlling M. gulosa in the USA. Additional control programs may be required to minimise the impact of M. gulosa on host plants. Existing domestic programs may provide some effectiveness for some hosts such as in cases where broad spectrum pesticide applications are utilised. However, this may not be the case for all hosts, particularly where specific integrated pest management programs are in place. In addition, potential biological control species may not be present in Western Australia. Existing IPM programs may be disrupted because of the need to re-introduce or increase the use of certain pesticides. This may result in increased production costs which may be incurred by the producer.
Domestic trade	D – Significant at the district level The presence of M. gulosa in commercial production areas may have a significant effect at the district level due to any resulting interstate trade restrictions on potentially a wide range of commodities. These restrictions may lead to either a loss of markets or require additional measures to facilitate ongoing trade.
International trade	C – Significant at the local level The presence of M. gulosa in commercial production areas of a range of commodities that are hosts may limit access to overseas markets where M. gulosa is absent.
Environmental and non-commercial	B – Minor at the local level While existing pest management practices may contain M. gulosa, additional pesticide applications and other control activities would be required to manage M. gulosa on susceptible crops. Any additional insecticide usage may affect the environment.

1.15.6Unrestricted risk estimate

Unrestricted risk is the result of combining the probability of entry, establishment and spread with the estimate of consequences. Probabilities and consequences are combined using the risk estimation matrix shown in Table 2.5.

Unrestricted risk estimate for Marmara gulosa
Overall probability of entry, establishment and spread	Low
Consequences	Low
Unrestricted risk	Very low

As indicated, the unrestricted risk estimate for Marmara gulosa has been assessed as ‘very low’, which achieves Australia’s ALOP. Therefore, no specific risk management measures are required for this pest.